Advances in Comparative and Environmental Physiology 10

Editor-in-Chief

R. Gilles, Liege

Editorial Board

P. 1. Butler, Birmingham R. Greger, Freiburg Ch.P. Mangum, Williamsburg G.N. Somero, Corvallis K. Takahashi, Tokyo R.E. Weber, Aarhus

Volumes already published

Vol. 1: NaCl ltansport in Epithelia Edited by R. Greger (1988)

Vol. 2: From the Contents: Hibernation - Vapor Absorption Nutrient Transport - Stable Pollutants (1988)

Vol. 3: Molecular and Cellular Basis of Social Behavior in Vertebrates Edited by J. Balthazart (1989)

Vol. 4: Animal Adaptation to Cold Edited by L. eH. Wang (1989)

Vol. 5: From the Contents: Osmoregulation - Chemoreception -Temperature - Spectroscopy - Metalloproteins Prostaglandins (Eicosanoids) -Maternal-Fetal Relationships (1989)

Vol. 6: Vertebrate Gas Exchange: From Environment to Cell Edited by R. G. Boutilier (1990)

Vol. 7: From the Contents: Protein Turnover -Xenobiotic Metabolism Lipoproteins (1991)

Vol. 8: From the Contents: Dormancy in Aquatic Invertebrates -Root Effect - Red Blood Cell Functions in Fish -Diving Mammals (1991)

Vol. 9: Volume and Osmolality Control in Animal Cells Edited by R. Gilles, E. K. Hoffmann, and L. Bolis (1991)

Vol. 10: Comparative Aspects of Mechanoreceptor Systems Edited by F. Ito (1992)

Vol. 11: Mechanics of Animal Locomotion Edited by R. MeN. Alexander (1992)

Volumes in preparation

Vol. 12: Muscle Contraction and Cell Motility: Molecular and Cellular Aspects Edited by H. Sugi (1992)

Vol. 13: Blood and Tissue Oxygen Carriers Edited by Ch. P. Mangum (1992)

Advances in

Comparative and Environmental Physiology 10 Comparative Aspects of Mechanoreceptor Systems

Guest Editor: F. Ito

With Contributions by J. Adler· M. Buechner· M.W. Chapleau· J.w. Deitmer A.H. Delcour· N. Fujitsuka· M.H. Gladden· M.e. Gustin W. Hamann· F. Ito • C. Kung· B. Martinac • H. Ohmori B.G. Pickard· J. Ping Ding· H. Romer· B. Rydqvist F. Sachs· M. Sokabe· J. Tautz • J.G. Widdicombe

With 111 Figures

Springer-Verlag Berlin Heidelberg New York London Paris Tokyo Hong Kong Barcelona Budapest

Guest Editor:

Professor Fumio Ito Department of Physiology School of Medicine Nagoya University 65 Tsurumai-cho, Showa-ku Nagoya, Japan

ISBN-13: 978-3-642-76692-3 e-ISBN-13: 978-3-642-76690-9 DOl: 10.1007/978-3-642-76690-9

Library of Congress Cataloging-in-Publication Data Comparative aspects of mechanoreceptor systems I editor, F. Ito. p. cm. - (Advances in comparative and environmental physiology; 10) Includes bibliographical references and index. ISBN-13: 978-3-642-76692-3 1. Mechanoreceptors. 2. Physiology, Comparative. 3. Ion channels. I. Ito, Fumio, 1929- . II. Series. QL938.M4C66 1992 591.1'8 - dc20 191-32197 CIP

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©Springer-Verlag Berlin Heidelberg 1992 Softcover reprint of the hardcover 1st edtion 1992

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Foreword to the Series

The aim of the series is to provide comprehensive, integrated reviews giving sound, critical and provocative summaries of our present know­ledge in environmental and comparative physiology, from the molecular to the organismic level.

Living organisms have evolved a widespread range of basic solutions to cope with the different problems, both organismal and environmental, with which they are faced. A clear understanding of these solutions is of course of fundamental interest for all biologists, zoologically or medically oriented. They can be best comprehended in the framework of the environmental and/or comparative approaches. These approaches demand either wide surveys of animal forms or a knowledge of the specific adaptive features of the species considered. This diversity of requirements, both at the conceptual and technological level, together with the fact that physiology and biochemistry have long been mainly devoted to the service of medicine, can account for the fact that these approaches emerged only slowly amongst the other new, more rapidly growing disciplines of the biological sciences.

The field has now gained the international status it deserves and the organization of a series devoted to it appeared timely to me in view of its actual rapid development and of the interest it arouses for a growing number of biologists, physiologists, and biochemists, independently of their basic, major orientation.

Liege, Belgium Raymond Gilles

List of Editors

Editor-in-Chief

R Gilles Laboratory of Animal Physiology University of Liege 22, Quai Van Beneden 4020 Liege, Belgium

Editorial Board

P.J. Butler School of Biological Sciences University of Birmingham P.O. Box 363 Birmingham B15 2TT, England

R Greger Physiologisches Institut der UniversiHit Freiburg Lehrstuhl II Hermann-Herder-Strasse 7 7800 Freiburg, FRG

Ch.P. Mangum Department of Biology The College of William & Mary Williamsburg, VA 23 185, USA

G.N.Somero Department of Zoology Oregon State University Corvallis, OR 97331-2914, USA

K. Takahashi Zoological Institute Faculity of Sciences University of Tokyo Hongo, Tokyo 113, Japan

RE. Weber Zoophysiology Laboratory University of Aarhus Building 131 8000 Aarhus C, Denmark

Those interested in contributing to this series should contact Professor R. Gilles or one of the Series Editors. Review proposals should include a short outline - and a Table of Contents - briefly defining the aims and scope of the review.

Preface

In the past 5 years there has been an enormous increase of evidence that the ion channels activated by mechanical force are common to a wide variety of cell types. Mechanosensitive (MS) ion channels form a small proportion of the total channel population. They are now found in more than 30 cell types from E. coli, yeast, to plant, invertebrate, and vertebrate cells, where they occur in virtually all types of cells from bone to smooth muscle, as well as neurons. The majority of MS channels are permeable to monovalent cations and are slightly selective for K+ over Na +. How­ever, there are several reports of anion-selective MS channels, MS Ca2+

channels, and MS channels with large conductances that do not dis­criminate markedly between cations and anions.

Recently B. Hille has postulated possible evolutionary relationships between several types of ion channels, with mechanosensitive channels predating even the eukaryotes. Two voltage-gated channel types originate with the stem eukaryotes, as deduced from the presence of voltage-gated K+ and Ca2+ channels in protozoa, algae, or higher plants. Agonist-gated chan­nels as well as voltage-gated Na + channels appear with the earliest metazoan animals, as deduced from the presence of Na + spikes and fast chemical synapses in cnidaria (coelenterates), ctenophores, and all higher animals.

MS channels have been found in specialized mechanoreceptors such as the crayfish stretch receptor neuron, although most studies have been performed on cell types for which there is no established role for mechanotransduction, such as skeletal muscle fiber. However, there is no evidence for many kinds of mechanoreceptors as to whether the transduction is attributable to the MS channels, because the sensory terminals are too small and too complicated to apply patch-clamp recovering. Thus, the available approach so far is to compare the kinetics of sensory reception in different kinds of mechanosensory organs of various kinds of animal. This approach should allow us to extend our knowledge about the interrelation between MS channels and the proper­ties of mechanoreceptors, the contribution of intracellular second mes­sengers to signal transduction, as well as the metabolism of the receptor channels and their genetic regulation

Nagoya, Japan, January 1992 Fumio Ito

Contents

Part I Mechanosensitive Ion Channels

Chapter 1

Mechanosensitive Ion Channels in Bacteria Bo Martinac, A.H. Delcour, Mo Buechner, 10 Adler, and C Kung

1 2

Introduction Mechanosensitive Ion Channels in Escherichia coli

3 Mechanosensitive Ion Channels in Other Bacteria 4 Perspective References 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

Chapter 2

Mechanosensitive Ion Channels in Yeast. Mechanisms of Activation and Adaptation MoC Gustin

1 2

Introduction Mechanisms of Activation of Mechanosensitive Channels

3 Mechanisms of Adaptation

o 3 o 4 o 14 o 16 o 17

019

020

of Mechanosensitive Channels 0 27 4 Physiological Function of Mechanosensitive Channels

in Walled Organisms 0 29 5 Summary 0 35 References 0 0 0 0 0 0 0 0 0 35

x

Chapter 3

Mechanosensory Transduction in Ciliates (Protozoa) 1. W. Deitmer

Contents

1 Mechanoreception and Cellular Behaviour . . . . . . . . . . . . 39 2 Physiological Responses to Mechanical Stimulation .... . 40 3 Properties of Mechanosensitive Ion Channels .......... 42 4 Electrical Excitation: Voltage-Dependent Ion Channels . . . . . 46 5 The Significance of Ion Channel Localization .......... 49 6 Concluding Remarks . . . . . . . . . . . . . . . . . . . 52 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 52

Chapter 4

Towards Molecular Mechanism of Activation in Mechanosensitive Ion Channels M. Sokabe and F. Sachs

1 Introduction ........................ . 55 2 Difficulties in Studying Mechanosensitive Ion Channels . 57 3 Analysis of SA Channel Gating Kinetics ...... . 59 4 Thermodynamic Models for SA Channel Gating . 63 5 Measurement of Membrane Tension . . . . . . . . . . . . . . . . 68 6 Conclusions and Future Perspectives ............... 75 References ................................. 76

Part n Mechanoreceptor Organs

ChapterS

Gravity Sensing by Higher Plants B. G. Pickard and 1. Ping Ding

1 Introduction ......................... . 2 Mechanically Activated Channels in a Model Plant System 3 Possible Ways to Open Gravitransductive Channels . . . . 4 Distribution of Mechanical Stress and Channel Activation 5 Activation of Auxin Porters ........ . 6 Load-Bearing at the .Cell Wall Level ........ . 7 Is Gravitropic Stress-Sensing an Expression

of a More General Growth-Regulating System? 8 Hydrostatic Pressure . . . . . . . . . . . . . . . .

.82

.83

.90

.93 .. 96 . .98

102 103

Contents

9 Statoliths References . .

Chapter 6

Mechanoreceptors in Respiratory Systems 1. G. Widdicombe and G. Sant'Ambrogio

XI

104 106

1 Introduction ......................... 112 2 Upper Airway Receptors .................. 112 3 Mechanoreceptors of the Respiratory Muscles and Joints 120 4 Lower Respiratory Tract and Lungs 124 5 Conclusions 132 References . . . . . . . . . . . . . . . . . 133

Chapter 7

Cardiovascular Mechanoreceptors M. W Chapleau

1 2 3 4

Introduction Location and General Function of Arterial Baroreceptors Mechanisms of Activation of Baroreceptors Influences of Pulsatile Pressure and Flow on Baroreceptor Discharge

5 Adaptation and Resetting of Baroreceptors 6 Summary References . . . . . . . . . . . . . . . . . . . . .

Chapter 8

Comparative Physiology of Cutaneous Mechanoreceptors WHamann

1 History ................ . 2 Types of Receptors . . . . . . . . . . . 3 Special Features in Different Species 4 Mechanical Properties and Method of Stimulation 5 Sympathetic Control of Mechanoreceptors References . . . . . . . . . . . . . . . . . . . . . . . . .

138 138 139

147 151 158 159

165 167 176 177 179 180

XII

Chapter 9

Invertebrate Auditory Receptors H. Romer and 1. Tautz

Contents

1 Introduction ........................ 185 2 Basic Structure and Physiology of Auditory Receptors 186 3 Airborne Sound Receptors . . . . . . . . . . . . . . . . 190 4 Vibration Receptors . . . . . . . . . . . . . . . . . . . . . . . . 198 5 Selected Reading . . . . . . . . . . . . . . 207 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 207

Chapter 10

Mechanoelectrical Transduction in Vertebrate Hair Cells H.Ohmori

1 Introduction ............. 213 2 Electrophysiology of Hair Cells 214 3 Mechanoelectrical Transduction .. 216 4 Muscarinic Cholinergic Receptor Mechanism

Might Mediate the Efferent Innervation to the Hair Cell 227 5 Length Change of the Guinea Pig Outer Hair Cell . . . . 230 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 230

Chapter 11

Muscle Mechanoreceptors in Invertebrates B. Rydqvist

1 Introduction ................... 234 2 Occurrence, Location and Gross Morphology

of Muscle Receptors . . . . . . . . . . . . . . . 235 3 Fine Structure and Organization of Muscle Receptor Organs 240 4 Functional Properties of Muscle Receptor Organs . . . . . . . 243 5 Summary 255 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 256

Chapter 12

Muscle Mechanoreceptors in Nonmammalian Vertebrates F. Ito, M. Sokabe, and N. Fujitsuka

1 Introduction ............................ 261 2 Spindle Preparation and Parameters of Sensory Axon Terminal . 263

Contents

3 Distinction Between Spindle Potential and the Actual Receptor Potential .. ...

4 The Site of Origin and Supposed Role of the Spindle Potential ....... .

5 A Model of Primary Processes in Sensory Encoding 6 Transduction and Mechanosensitive Channel:

Ultrastructural Aspects of Frog Muscle Spindle 7 Second Messengers in Transduction

and Encoding Processes References . . . . . . . . . . . . . . . . .

Chapter 13

Muscle Receptors in Mammals M.H. Gladden

1 Introduction ................ . 2 Types of Intrafusal Muscle Fibre ..... . 3 Fusimotor Innervation - The Basic Pattern 4 Effects of Contraction

of Intrafusal Fibres on Spindle Sensory Endings 5 Nonselectivity and the Subdivision of Static y-Axons 6 Summary and Conclusions References . . . . . . . . . . . . . . . . . . . . . . . . . .

XIII

263

266 268

270

273 276

281 283 286

286 293 298 299

Subject Index .............................. 303